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Home , Aldrovanda, Cephalotus, Nepenthes, Tendril, Venus flytrap

& MEDICINE_Plant Research

Fill up the bowl!

Leghold traps, limed rods, pit traps - insectivorous have come up with unusual strategies to obtain additional nutrients. Axel Mithöfer at the Max Planck Institute for Chemical Ecology in Jena is investigating how pitcher plants from Southeast Asia entrap and digest their victims.

TEXT CATARINA PIETSCHMANN

lants that consume animals – there are also purely practical ways of us- That’s why, if you have a carnivorous imagine coming up with an ing them. In , for example, the at home, you shouldn’t fertilize idea like that! Evolution, traps of the , , are it. “If they can meet their needs for nu- though, doesn’t suffer from filled with sticky rice, vegetables, or trients using their roots, they form qualms. Pitcher plants are ex- meat and eaten. On the island of Bor- fewer traps and instead invest more traordinaryP and have long been a source neo, old pitchers that have lignified are energy in for ,” of curiosity and flights of fantasy. used as storage vessels for food and explains Mithöfer. Charles Darwin went as far as to drink or for steaming rice. Of all the insectivorous plants, the dedicate an entire book to these plants, , Dionaea muscipula, with commonly referred to as carnivorous. FLUID WITH MEDICINAL POWERS its traps reminiscent of leghold traps, is Of the sundew’s trapping mechanism, the most spectacular. It is native to he wrote: “It is surprising how minute The plants are even said to be good for North American and is the best a particle of any substance, ... if placed your health. Indigenous peoples, for ex- known active trapper. The waterwheel in actual contact with the surface of a ample, treat skin inflammations and di- plant, , indigenous in Ger- gland, suffices to cause the tentacle to gestive disorders with the digestive liq- many but now extinct there, does pos- bend. [...] It is a much more remarkable uid from the pitchers. sess a very similar trapping mechanism fact that when an object, such as a bit Axel Mithöfer also has a practical to the Venus flytrap. Its leaves, howev- of meat or an , is placed on the use for insectivorous plants. “In sum- er, are only a few millimeters in size, disc of a , as soon as the surround- mer, I place two or three sundew plants and the plant grows under water, mak- ing tentacles become considerably in- next to the fruit bowl. That deals with ing it relatively unknown. With its ten- flected, their glands pour forth an in- any problems with fruit .” tacles that twist around its prey, the creased amount of secretion.” The additional nutrition the plants sundew is also an active trapper. It’s not just our fascination with get from animals helps them to keep The Venus flytrap snaps shut on

plant that have attracted us; up in nutrient-poor environments. its victims at a surprising speed for a Photo: Anna Schroll

60 MaxPlanckResearch 2 | 19 Under UV light, the trap of a pitcher plant resembles a filigree work of art. are attracted by on the rim of the pitcher and slip into the belly of the trap. The lid prevents rain from diluting the digestive fluid in the trap. Photo: Anna Schroll BIOLOGY & MEDICINE_Plant Research

Chitin receptors signal the presence of prey to the pitcher plants » – in the true sense of the word, they taste their food.

plant. Mithöfer gives me a demonstra- and digestive juices are secreted from of the Venus flytrap, and Mithöfer’s tion of the trapping mechanism in the glands in the trap, bathe the prey and team already possess that of one pitch- greenhouse of the Max Planck Institute dissolve it. The same glands then ab- er plant of the Nepenthes. in Jena. He carefully strokes a fine twig sorb what the hungry plant lacks in its over an open trap, touching the tactile nutrient-poor : and NEW TASKS FOR trigger hairs inside it a few times. The phosphate compounds. plant has three of these hairs, barely The feast lasts several days. Then From their genes, it’s clear that carniv- visible to the naked eye, on each half the trap unfolds again and spits out the orous plants have important things in of the trap leaf. “bones” – the indigestible exo- common, even if they developed the skeleton of the . In the wild, the next ability differently. They all use the en- STRUGGLING IS DEADLY rain shower washes out the remains of zymes that evolution passed them down the banquet. from their ancestors. “Plants have been The trap snaps shut in a tenth of a sec- The sundew does things entirely dif- exposed to herbivores and pathogens, ond. “If the fly were smart, it would ferently. If an insect lands on its leaves, such as fungi, for 400 million years. stay motionless for two hours. The trap which are covered with fine tentacles, And that’s the reason why they devel- would then open, and it could fly off,” it gets trapped by countless droplets of oped enzymes like that can explains Mithöfer. But staying standing a sticky liquid. After this, the tentacles break down the cell walls of fungi,” said still isn’t in the nature of flies. Under- at the edge of the leaf first maneuver Axel Mithöfer. standing why isn’t hard. Caught be- the animal into the middle of the leaf, It’s a fortunate coincidence that tween the trap leaves, it panics and where many of the glands that produce the carapace of insects is also made of struggles wildly to free itself. digestive juice are located. The leaf then chitin. Carnivorous plants take advan- Each time it touches a trigger hair, slowly curls over the “meal”, and the tage of this fact and simply re-deploy it generates a tiny electrical impulse, prey is digested. their existing tools, turning defensive just like that in a nerve cell. “The plant There have been multiple indepen- enzymes into digestive secretions. sums the impulses to determine if it dent instances of plants developing They can now use chitinases to has actually caught living prey, or if ways to consume animals. Depending break down the chitin shells of insects only a drop of rain has landed on it,” on the expert you ask, there have been and get at the nutrients within. The Mithöfer explains. “Two, three con- four to nine separate lines of develop- plants get the nitrogen and phosphate tacts are okay. But nine or ten means ment. The genomes of some species from the bodies of the insects using it’s curtains for the fly!” A plant that such as of a bladderwort, proteins and enzymes that digest nu- can actually count! gibba, and the Australian Albany pitch- cleic acids. While the trap leaves squeeze to- er plant, , have already been Mithöfer’s particular field of exper- gether tightly and crush the insect, the deciphered. In Wuerzburg, researchers tise is pitcher plants. There are just over

flytrap literally starts to salivate. Acid are currently working on the genome 120 species of the genus Nepenthes in Photos: Anna Schroll (3)

62 MaxPlanckResearch 2 | 19 Above left The Venus flytrap has a sophisticated capture mechanism. The leaves have been repurposed as folding traps and contain trigger hairs, which send signals to the plant when an insect is trapped. Within fractions of a second, the two leaf halves snap shut and capture the prey. Above right The various species of sundew – here the Cape sundew – in contrast rely on sticky traps. Looking like sweet nectar on red glittering in the sunlight, the traps are actually covered with a sticky liquid designed to attract and hold insects. Below Alberto Dávila-Lara is a doctoral student in Axel Mithöfer’s research group. The photograph shows him collecting nectar from the rim of a pitcher. Photos: Anna Schroll (3)

2 | 19 MaxPlanckResearch 63 the humid tropical rain forests of At its rim, the pitcher secretes nectar, “We do that to prevent flies from escap- Southeast Asia, most of them, climbing which becomes exceptionally slippery at ing or something else from falling into plants. Four species of Nepenthes grow high . There’s no way of grip- the pitcher.” in the greenhouse of Mithöfer’s Insti- ping, even using the fine adhesive pads And how do the pitchers sense that tute in Jena. of insects feet. Incautious insects fall and prey is near? Unlike the Venus flytrap, Pitcher plants primarily prey on soil drown in the fluid of the pitcher. Nepenthes produces chemical rather insects such as and . After Axel Mithöfer investigates how di- than electrical signals. The plant’s traps a pitcher has matured and filled to a gestive secretions are generated by feed- probably have receptors for chitin – the good quarter with fluid, the lid opens ing the pitchers with fruit flies and substance that forms the carapace of and the “hunting season” commences. then placing nylon socks over them. insects. While other plants use recep-

Above Using a sterile syringe, Alberto Dávila-Lara extracts digestive fluid from an unopened pitcher for further analysis. Below left A fluorescence microscope reveals the glands in the pitcher wall that produce the digestive fluid. Below right The glands lie in depressions of the epidermis and are covered by protruding hoods (The bar corresponds to one-twentieth of a millimeter). Photos: Anna Schroll (above), MPI for Chemical Ecology (below, 2)

64 MaxPlanckResearch 2 | 19 BIOLOGY & MEDICINE_Plant Research

Simple leaf Nepenthes leaf

Leaf base

Leaf base = /stalk = Lamina lamina-shaped structure

Petiole Lamina = pitcher

Metamorphosis from leaf to trap: over the course of evolution, the leaf base of an ordinary leaf in Nepenthes has developed into a basal structure and the petiole into the tendril of the pitcher. The leaf lamina eventually developed into the actual trap.

tors to detect predators, pitcher plants on the body of the pitchers are not only as long as possible. If too many insects use theirs to sense the presence of prey. sweet, they also glow violet under black are caught, the plant can no longer pre- So, in the true sense of the word, they light in the laboratory. Chemical anal- vent bacteria from proliferating in the taste their food. ysis of the nectar revealed that this is pitcher fluid. When this happens, the probably due to a flavonoid. “Maybe trap is broken down and discarded. CHITIN PROMOTES it’s this glow that attracts the insects,” says Mithöfer. LEAVES CONVERTED INTO TRAPS “As soon as the receptors detect the To prove their hypothesis, Mithöfer chitin of an insect’s carapace, a signal and his team intend to test the behav- Even if the pitchers are usually striking- cascade is triggered that activates the ior of ants by comparing how they be- ly colored and patterned, they’re not production of digestive enzymes,” says have presented with natural Nepenthes the flowers, but elongated, widened, Mithöfer. One of the cascade’s most im- nectar and then with an artificial nec- and specialized leaves – a beautiful ex- portant signaling substances is the phy- tar lacking the flavonoid. To perform ample of how plant leaves can perform tohormone jasmonic acid, which is also the experiment, they plan to fly an en- a variety of tasks. They hang from the used to defend against predators. The di- tire colony, including the queen, plants in all stages of development: un- gestive enzymes originate from glands from to Jena. ripe and closed, active with the lid open, in the lower third of the pitcher. These The pitcher fluid does already con- and shriveled and dead. If a pitcher is glands have two functions. “They both tain small amounts of enzymes before incapable of consuming food, it is usu- exude secretions and also transport the the first prey lands in it. But it can take ally only discarded when the plant has nutrients from the prey into the plant.” between two and three days for enough extracted as many nutrients as possible Typically, it’s in their flowers that digestive enzymes to form. “Nepenthes from it. A pitcher plant, after all, doesn’t plants secrete nectar; Nepenthes, on the can take its time; the prey isn’t going have resources to spare. other hand, generates it at the rims of anywhere. It’s a real gourmet!” Not all carnivorous plants catch its pitchers. And the nectar isn’t used to Mithöfer’s team extracted the fluid their own food. Some have a “delivery attract pollinators, but, instead, to from still young, unopened pitchers service” and reward the couriers with catch prey. Unlike nectar, which and discovered potassium chloride, sweet rewards. There are also Nepen- can contain aromatic substances, pitch- trace elements, digestive enzymes, and thes species that provide shelter for er nectar is entirely odorless. Even so, naphthoquinones. As soon as the trap ants. They live sheltered in cavities of ants and beetles are tremendously at- has caught something, it produces addi- the pitcher plant and, in return, de- tracted to it. tional digestive enzymes and acid to ac- fend their landlady against predators. Mithöfer’s doctoral student Alberto tivates the enzymes. The naphthoqui- They themselves are unaffected by the Dávila-Lara discovered that the rim of nones have an antimicrobial effect and digestive juices, which they simply

Photos: Anna Schroll (above), MPI for Chemical Ecology (below, 2) Graphic: MPI for Chemical Ecology pitchers and the dot-like nectar glands probably keep the juice free of germs for swim through. >

2 | 19 MaxPlanckResearch 65 BIOLOGY & MEDICINE_Plant Research

“Insight must precede application.” Max Planck

The Max Planck Society is a world-leading insti- tution pursuing basic research in a wide area of sciences and humanities. Research is performed

at Max Planck Institutes ↘ within Germany and at a few other locations world-wide. Directors lead an institute jointly with their fellow directors and pursue a bold research agenda within their Axel Mithöfer is investigating independent departments. the signal cascades used by plants to protect themselves from predators and pathogens. The Max Planck Society is seeking nominations for Insectivorous plants have modified some of the molecules in the cascades to turn themselves into preda- tors. A bushy angelica grows in the tea room of Mithöfer’s MAX PLANCK DIRECTORS research group, but ... it wouldn’t harm a fly.

We are looking for the strongest and most To nominate an outstanding scientist, please The plant also benefits from extracting creative scientists worldwide. Core criteria for provide a letter of support. For self-nominations, the valuable nutrients from the waste directorship are scientific and scholarly excel- please upload a letter of motivation including material of the ants. In some instances, SUMMARY lence, an innovative and visionary research a two to three page research proposal, your this type of nutrition can take on biz- l There have been multiple instances of plant species independently evolving program, and personal and intellectual leader- CV, a publication list and three to five selected zare forms. “On the island of , as carnivores to consume insects. ship, rather than seniority. Max Planck Directors publications. tree shrews and rats sit on the rim of l Few plants species have evolved the ability to eat insects as new inventions; enjoy complete scientific freedom. We offer an particularly large pitchers of certain instead, they have tended to repurpose existing tools. international and excellent research environ- For online nominations and more information Nepenthes species, lick sweet nectar l Pitcher plants do not attract insects with the smell of the nectar they secrete

ment, outstanding infrastructure, and compe- including a list of Max Planck Institutes, please from the inner surface of the lid – and on the rim of their pitchers. Instead, the nectar reflects ultraviolet light, and ↘ simultaneously release their droppings this is probably what attracts insects. titive long-term scientific funding. Excellent visit the * Nomination Portal URL* . into the pitcher. Another Nepenthes administrative support enables our directors to species provides daytime shelter for focus on research. Nominations should be submitted by 28 Oct. 2019 bats, whose excrement they then uti- GLOSSARY lize,” Mithöfer explains. The Max Planck Society strives for gender equity Nominations will be treated with strictest confi- Besides carnivores and excrement Pitcher plants: At present about 120 Nepenthes species are known, and researchers are and welcomes nominations of candidates with dentiality and later nominations may also be feeders, pitcher plants can even be her- still discovering new species. Their range extends from to and from to Northern . The leaves consist of a leaf base, a tendril, and diverse backgrounds. We actively encourage considered. bivores. with its the actual pitcher trap. Some species have traps up to 50 centimeters in size. Many nominations of persons with disabilities. large pitcher openings, for example, Nepenthes species are threatened with due to loss of habitat and illegal trade. waits for leaves to fall into its pitcher. Venus flytrap: The traps of these carnivorous plants capture insects by snapping shut A plant that, during the course of on them, after which they begin by exposing them to hydrochloric acid from gland evolution, consumes first light, then cells. After a delay of a few hours, the glands also release digestive enzymes. The bro- animals, and finally other plants – ken down nutrients are then absorbed by the same glands. These glands, are therefore similar in function to roots. This explains why only those genes that are typical for both Nomination portal: could there be any better way of leaves and roots are active in the trap cells. https://www.mpg.de/career/commoncall demonstrating nature’s almost infinite

versatility? Photo: Anna Schroll

66 MaxPlanckResearch 2 | 19 Photo: Anna Schroll MAX PLANCK DIRECTORS nominations ofpersonswithdisabilities. diverse backgrounds. We actively encourage and welcomesnominationsofcandidateswith The MaxPlanckSocietystrives forgender equity focus onresearch. administrative enablesourdirectors to support titive long-termscientificfunding. Excellent ment, outstandinginfrastructure, andcompe- international andexcellent research environ- enjoyfreedom.scientific complete We offer an ship, rather thanseniority. MaxPlanck Directors program, andpersonalintellectual leader- lence, aninnovative research andvisionary directorship are scientificandscholarlyexcel- creative scientistsworldwide.Core criteriafor We are lookingforthestrongest andmost The MaxPlanck Society isseeking nominationsfor precedeapplication.” “Insight must independent departments. and pursueaboldresearch agendawithintheir lead aninstitutejointlywiththeirfellow directors at afew otherlocationsworld-wide. Directors at sciences andhumanities.Research isperformed tution pursuingbasicresearch inawidearea of The MaxPlanckSocietyisaworld-leadinginsti- * Nomination Portal URL* visit the* NominationPortal including alistofMaxPlanckInstitutes,please Forand moreonline nominations information publications. CV, apublicationlistandthree to five selected a twoto three pageresearch proposal, your please uploadaletterofmotivation including Forprovide self-nominations, aletter ofsupport. To nominateanoutstandingscientist,please considered. dentiality andlaternominationsmay alsobe Nominations willbetreated withstrictestconfi- be submittedbyshould Nominations https://www.mpg.de/career/commoncall Nomination portal: Max Planck Institutes ↘ within Germanyand ↘ 28 Oct. 2019 Max Planck .